Skip to main content
SpringerLink
Log in

The in-vivo response of the ribulose-1,5-bisphosphate carboxylase activation state and the pool sizes of photosynthetic metabolites to elevated CO2 inPhaseolus vulgaris L.

  • Published:
Planta Aims and scope Submit manuscript

Abstract

The short-term, in-vivo response to elevated CO2 of ribulose-1,5-bisphosphate carboxylase (RuBPCase, EC 4.1.1.39) activity, and the pool sizes of ribulose 1,5-bisphosphate, 3-phosphoglyceric acid, triose phosphates, fructose 1,6-bisphosphate, glucose 6-phosphate and fructose 6-phosphate in bean were studied. Increasing CO2 from an ambient partial pressure of 360–1600 μbar induced a substantial deactivation of RuBPCase at both saturating and subsaturating photon flux densities. Activation of RuBPCase declined for 30 min following the CO2 increase. However, the rate of photosynthesis re-equilibrated within 6 min of the switch to high CO2, indicating that RuBPCase activity did not limit photosynthesis at high CO2. Following a return to low CO2, RuBPCase activation increased to control levels within 10 min. The photosynthetic rate fell immediately after the return to low CO2, and then increased in parallel with the increase in RuBPCase activation to the initial rate observed prior to the CO2 increase. This indicated that RuBPCase activity limited photosynthesis while RuBPCase activation increased. Metabolite pools were temporarily affected during the first 10 min after either a CO2 increase or decrease. However, they returned to their original level as the change in the activation state of RuBPCase neared completion. This result indicates that one role for changes in the activation state of RuBPCase is to regulate the pool sizes of photosynthetic intermediates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

A :

net CO2 assimilation rate

Ca :

ambient CO2 partial pressure

Ci :

intercellular CO2 partial pressure

CABP:

2-carboxyarabinitol 1,5-bisphosphate

kcat :

catalytic turnover rate per RuBPCase molecule

PFD:

photon flux density (400 to 700 nm on an area basis)

PGA:

3-phosphoglyceric acid

Pi :

orthophosphate

RuBP:

ribulose 1,5-bisphosphate

RuBPCase:

ribulose-1,5-bisphosphate carboxylase (EC 4.1.1.39)

References

  • Belknap, W.R., Portis, A.R. Jr. (1986) Exchange properties of the activator CO2 of spinach ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol.80, 707–710

    Google Scholar 

  • Collatz, G.J., Badger, M.R., Smith, C., Berry, J.A., (1979) A radioimmune assay for RuP2 carboxylase protein. Carnegie Instn. Washington Yearb.78, 171–175

    Google Scholar 

  • Dietz, K.-J. (1985) A possible rate-limiting function of chloroplast hexosemonophosphate isomerase in starch synthesis in leaves. Biochim. Biophys. Acta839, 240–248

    Google Scholar 

  • Dietz, K.-J., Heber, U. (1984) Rate limiting factors in photosynthesis. I. Carbon fluxes in the Calvin cycle. Biochim. Biophys. Acta767, 432–443

    Google Scholar 

  • Farquhar, G.D., von Caemmerer, S. (1982) Modelling of photosynthetic response to environmental conditions. In: Encyclopedia of plant physiology, N.S., vol 12B: Physiological plant ecology II, pp. 549–587, Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H., eds. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Gerhardt, R., Stitt, M., Heldt, H.W. (1987) Subcellular metabolite levels in spinach leaves. Regulation of sucrose synthesis during diurnal alterations in photosynthetic partitioning. Plant Physiol.83, 399–407

    Google Scholar 

  • Harris, G.C., Cheesbrough, J.K., Walker, D.A. (1983) Effects of mannose on photosynthetic gas exchange in spinach leaf discs. Plant Physiol.71, 108–111

    Google Scholar 

  • Herold, A. (1980) Regulation of photosynthesis by sink activity — the missing link. New Phytol.86, 131–144

    Google Scholar 

  • Hoagland, D.R. and Arnon, D.I. (1938) The water culture method for growing plants without soil. Univ. Cal. Agric. Expt. Stat. (Berkeley) Circ. No. 347

  • Leegood, R.C., Furbank, R.T. (1986) Stimulation of photosynthesis at low temperatures is restored by phosphate. Planta168, 84–93

    Google Scholar 

  • McVetty, P.B.E., Canvin, D.T. (1986) Inhibition of photosynthesis by low oxygen concentrations. Can. J. Bot.59, 721–725

    Google Scholar 

  • Miziorko, H.M., Lorimer, G.H. (1983) Ribulose-1,5-bisphosphate carboxylase-oxygenase. Annu. Rev. Biochem.52, 507–535

    Google Scholar 

  • Mott, K.A., Berry, J.A. (1986) Effects of pH on activity and activation of ribulose 1,5-bisphosphate carboxylase at air level CO2. Plant Physiol.82, 77–82

    Google Scholar 

  • Mott, K.A., Jensen, R.G., O'Leary, J.W., Berry, J.A. (1984) Photosynthesis and ribulose 1,5-bisphosphate concentrations in intact leaves ofXanthium strumarium L. Plant Physiol.76, 968–971

    Google Scholar 

  • Perchorowicz, J.T., Raynes, D.A., Jensen, R.G. (1981) Light limitation of photosynthesis and activation of ribulose bisphosphate carboxylase in wheat seedlings. Proc. Natl. Acad. Sci. USA78, 2985–2989

    Google Scholar 

  • Preiss, J. (1982) Regulation of the biosynthesis and degradation of starch. Annu. Rev. Plant Physiol.33, 431–454

    Google Scholar 

  • Robinson, S.P., Walker, D.A. (1979) The site of sucrose synthesis in isolated leaf protoplasts. FEBS Lett.107, 295–299

    Google Scholar 

  • Sage, R.F. (1986) Photosynthesis and nitrogen use efficiency of C3 and C4 plants. Ph.D. thesis, University of California, Davis, USA

    Google Scholar 

  • Sage, R.F., Seemann, J.R., Sharkey, T.D. (1987) Rate of deactivation and reactivation of ribulose-1,5-bisphosphate carboxylase in response to changing CO2 and O2 pressure. Progr. Photosynth. Res.3, 285–288

    Google Scholar 

  • Sage, R.F., Sharkey, T.D. (1987) The effect of temperature on the occurrence of O2 and CO2 insensitive photosynthesis in field grown plants. Plant Physiol.84, 658–664

    Google Scholar 

  • Salvucci, M.E., Portis, A.R., Ogren, W.L. (1986) Light and CO2 response of ribulose-1,5-bisphosphate carboxylase/oxygenase activation inArabidopsis leaves. Plant Physiol.80, 655–659

    Google Scholar 

  • Schnyder, H., Mächler, F., Nösberger, J. (1986) Regulation of ribulose 1,5-bisphosphate and ribulose 1,5-bisphosphate carboxylase/oxygenase activity associated with lack of oxygen inhibition of photosynthesis at low temperature. J. Exp. Bot.37, 1170–1179

    Google Scholar 

  • Seemann, J.R., Berry, J.A., Freas, S.M., Krump, M.A. (1985) Regulation of ribulose bisphosphate carboxylase activity in vivo by a light modulated inhibitor of catalysis. Proc. Natl. Acad. Sci. USA82, 8024–8028

    Google Scholar 

  • Seemann, J.R., Kobza, J. (1988) Genetic variation in the regulation of ribulose-1,5-bisphosphate carboxylase activity. Plant Physiol. Biochem. (in press)

  • Seemann, J.R., Sharkey, T.D. (1986) Salinity and nitrogen effects on photosynthesis, ribulose 1,5-bisphosphate carboxylase and metabolite pool sizes inPhaseolus vulgaris. Plant Physiol.82, 555–560

    Google Scholar 

  • Seemann, J.R., Sharkey, T.D. (1987) The effect of abscisic acid and other inhibitors on photosynthetic capacity and the biochemistry of CO2 assimilation. Plant Physiol.84, 696–700

    Google Scholar 

  • Seemann, J.R., Tepperman, J.M., Berry, J.A. (1981) The relationship between photosynthetic performance and the levels and kinetic properties of RuBP carboxylase-oxygenase from desert winter annuals. Carnegie Instn. Washington Yearb.80, 67–72

    Google Scholar 

  • Servaites, J.C. (1985) Binding of phosphorylated inhibitor to ribulose bisphosphate carboxylase/oxygenase during the night. Plant Physiol.78, 839–843

    Google Scholar 

  • Servaites, J.C., Perry, M.A.J., Gutteridge, S., Keys, A.J. (1986) Species variation in the predawn inhibition of ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol.82, 1161–1163

    Google Scholar 

  • Sharkey, T.D. (1985a) Photosynthesis in intact leaves of C3 plants: physics, physiology and rate limitations. Bot. Rev.51, 53–105

    Google Scholar 

  • Sharkey, T.D. (1985b) O2-insensitive photosynthesis in C3 plants. Its occurrence and a possible explanation. Plant Physiol.78, 71–75

    Google Scholar 

  • Sharkey, T.D., Seemann, J.R., Berry, J.A. (1986a) Regulation of ribulose-1,5-bisphosphate carboxylase in response to changing partial pressure of O2 and light inPhaseolus vulgaris. Plant Physiol.81, 788–791

    Google Scholar 

  • Sharkey, T.D., Stitt, M., Heineke, D., Gerhardt, R., Raschke, K., Heldt, W. (1986b) Limitation of photosynthesis by carbon metabolism. II. O2 insensitive CO2 assimilation results from triose phosphate utilization limitations. Plant Physiol.81, 1123–1129

    Google Scholar 

  • Sivak, M.N., Walker, D.A. (1986) Photosynthesis in vivo can be limited by phosphate supply. New Phytol.102, 499–512

    Google Scholar 

  • Stitt, M. (1986) Limitation of photosynthesis by carbon metabolism. I. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO2. Plant Physiol.81, 1115–1122

    Google Scholar 

  • Streusand, V.J., Portis, A.J. (1987) Rubisco activase mediates ATP-dependent rubisco activation. Plant Physiol.85, 152–154

    Google Scholar 

  • Taylor, S.E., Terry, N. (1984) Limiting factors in photosynthesis. V. Photochemical energy supply colimits photosynthesis at low values of intercellular CO2 concentrations. Plant Physiol.75, 82–86

    Google Scholar 

  • Taylor, S.E., Terry, N. (1986) Variation in photosynthetic electron transport capacity in vivo and its effects on the light modulation of ribulose bisphosphate carboxylase. Photosynth. Res.8, 249–256

    Google Scholar 

  • Viil, J., Laisk, A., Oja, V., Parnik, T. (1977) Enhancement of photosynthesis caused by oxygen under saturating irradiance and high CO2 concentrations. Photosynthetica11, 251–259

    Google Scholar 

  • von Caemmerer, S., Edmondson, D.L. (1986) The relationship between steady-state gas exchange, in vivo RuP2 carboxylase activity and some carbon reduction cycle intermediates inRaphanus sativus. Aust. J. Plant Physiol.13, 669–688

    Google Scholar 

  • von Caemmerer, S., Farquhar, G.D. (1981) Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. Planta153, 376–387

    Google Scholar 

  • von Caemmerer, S., Farquhar, G.D. (1985) Kinetics of activation of rubisco and some preliminary modelling of RuP2 pool sizes. In: Kinetics of photosynthetic carbon metabolism in C3-plants, pp. 46–59, Viil, J., Grishna, G., Laisk, A., eds. Valgus, Tallinn (USSR)

    Google Scholar 

  • Vu, C.V., Bowes, G., Allen, L.H. (1984) Dark/light modulation of ribulose bisphosphate carboxylase activity in plants from different photosynthetic categories. Plant Physiol.76, 843–845

    Google Scholar 

  • Walker, D.A., Sivak, M.N., Prinsley, R.T., Cheesbrough, J.K. (1983) Simultaneous measurement of oscillations in oxygen evolution and chlorophylla fluorescence in leaf pieces. Plant Physiol.73, 542–549

    Google Scholar 

  • Woo, K.C., Wong, S.C. (1983) Inhibition of CO2 assimilation by supraoptimal CO2: Effect of light and temperature. Aust. J. Plant Physiol.10, 75–85

    Google Scholar 

Download references

Author information

Author notes

  1. Rowan F. Sage

    Present address: Department of Botany, University of Georgia, 30602, Athens, GA, USA

  2. Thomas D. Sharkey

    Present address: Department of Botany, University of Wisconsin, 53706, Madison, WI, USA

  3. Jeffrey R. Seemann

    Present address: Department of Biochemistry, University of Nevada, 89557, Reno, NV, USA

Authors and Affiliations

  1. Biological Sciences Center, Desert Research Institute, P.O. Box 60220, 89506, Reno, NV, USA

    Rowan F. Sage, Thomas D. Sharkey & Jeffrey R. Seemann

Authors
  1. Rowan F. Sage
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas D. Sharkey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeffrey R. Seemann
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sage, R.F., Sharkey, T.D. & Seemann, J.R. The in-vivo response of the ribulose-1,5-bisphosphate carboxylase activation state and the pool sizes of photosynthetic metabolites to elevated CO2 inPhaseolus vulgaris L.. Planta 174, 407–416 (1988). https://doi.org/10.1007/BF00959528

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00959528

Key words

Search

Navigation